Exclusive Excerpt: Sex, Drugs and Sea Slime

Among the organisms of the oceans that are armed and dangerous, there is one elite group of jetsetters that grow fast and are blessed with brains, looks, and a talent for disguise. Though most don’t live long, they can react with lightning-quick speed and deploy amazing defensive countermeasures. They are the stars of film and literature, playing oversized and aggressive monsters with a killer appetite. Most of the oceans’ cephalopods, however, are not out for a fight; when trouble calls, the majority of squids, cuttlefishes, and octopuses prefer to hide or run away. They are also much stranger in fact than in fiction, with truly astonishing capabilities and many bizarre characteristics. Their diverse ranks have come a long way from their distant and rather simple cousin, the clam.

More than eight hundred species of cephalopods reside within the world’s oceans and include squids, octopuses, cuttlefishes, the nautilus, and a unique deep-sea crossover — the vampire squid. They are all mollusks, with a heredity distantly connected to shellfish such as clams, oysters, and snails. Oddly, what was once a foot evolved to become mostly a head along with a bevy of arms, and all but the nautilus lost their protective outer shells.

Cephalopods grow fast and most reach maturity within two years. To fuel their rapid growth, most squids, octopuses, and cuttlefishes are voracious and well-equipped hunters, feeding on live prey, such as crustaceans, fishes, shellfish, and other cephalopods. They have eight muscular, suckered arms, which they use to grab and immobilize their victims. Squids and cuttlefishes also have two longer, elastic tentacles that may be tipped with hooked clubs and can be deployed in an instant to lash out at potential victims, aka food. Suckers on a squid’s tentacles may be teethed for better gripping. Because cephalopods have relatively small mouths, these hunters must chop, drill, or soften up their catch before swallowing. To do this, they often use their hard, parrot-like beaks, which can tear apart flesh and crush bone. Within their mouths, they also have rasping tongues lined with small teeth, which some octopuses use to drill through their prey’s outer shell or exoskeleton. And cephalopods have acidic, venomous spit. Their salivary glands produce digestive enzymes and toxins, the latter of which vary in potency with species. The saliva of the small blue-ringed octopus contains one of the deadliest venoms on the planet. These potential “death spitters,” however, seem to be rather timid creatures and use their potent saliva mainly for feeding. A cephalopod’s spit is typically used to paralyze prey. When feasting on crabs, an octopus wields its spew with purpose. It drills a small hole into a crab’s carapace and then injects saliva to destroy its prey’s attachment muscles and begin the digestion process. And being picky, fastidious eaters, octopuses make the most of each meal. Piles of disarticulated shells or crustacean carapaces just outside an octopus’s lair are often picked clean of meat.

Most cephalopods use their excellent vision to hunt down their prey, but they are also able to feel out their victims or seek them through “smell” or chemical cues in the water. Some are also able to sense vibrations produced by an organism’s movements. Once prey is located, cephalopods are well outfitted for the chase. In the open ocean, a squid can outswim and outmaneuver many other animals. Its streamlined, torpedo-shaped body includes a jet-propulsion system that uses muscular contractions to force water into its mantle or bag-like body and out through a maneuverable pipe-like siphon, enabling the squid to become an agile, speedy jetfighter or stealthy hovercraft. Fins along its sides or rear are used for steering and stability, and sometimes for swimming. And when they go from hunter to huntee, some species of squid can even rocket out of the water and glide for up to 50 meters (164 feet) — though Hollywood has yet to produce Attack of the Killer Flying Squid. Though probably not as fast or as agile as squids, many cuttlefishes and octopuses also rely on in-body jet packs for swimming. In contrast, deep-water octopuses use fins for slow-motion sculling, and have webbing between their arms that acts like a parachute or sail. Octopuses that live on the bottom are extremely mobile creatures as well, which can crawl over just about any obstacle, can walk on their arms if need be, and are expert contortionists, able to squeeze through incredibly small openings while on the hunt or to avoid predators.

Hunting strategies vary among the cephalopods. An octopus may grab or pounce on its prey and then drag it back to its lair for stockpiling. As tactile feeders, they may poke and prod looking for food, or simply spread their arms or webbing out and eat whatever they find and capture. Other cephalopods, such as the squids, stealthily stalk their prey or choose a more direct approach and attack head-on, like a ballistic missile strike. With excellent skills at camouflage and mimicry, some of this group may also lure in unsuspecting prey. One deep-sea octopus has special suckers along the length of its arms that emit blue-green light. They may glow dimly or blink on and off, and are thought to attract potential quarry. Beneath its webbed arms, this octopus also produces mucus (seems like under the sea almost everyone does), which may ensnare small crustaceans that drift or swim into it, like a slimy net.

While on the hunt, cephalopods must always be wary of predators. Having lost the protection of an outer shell, their naked, soft bodies of- fer energy-rich, enticing meals. Just about every type of marine carnivore eats cephalopods, including whales, dolphins, seals, seabirds, and fishes such as the billfishes, tuna, groupers, and sharks. Even the cephalopods eat cephalopods.

To avoid the oceans’ hungry masses, cephalopods have developed an extraordinary array of defenses. Roger Hanlon of the Marine Biological Laboratory in Woods Hole, Massachusetts, has been studying cephalopods for decades. He discovered that when confronted, their first line of defense is camouflage, and that they are the fastest, best-equipped animals on the planet when it comes to hiding in plain sight. Occasionally, even he has been fooled by their amazing ability to disappear into their surroundings. Cephalopods are able to quickly and precisely take on the appearance of the bottom and become very uncephalopod-like. They can match the brightness, color, pattern, and texture of the seafloor in seconds, create optical illusions, and change the shape of their bodies to mimic in 3-D. Much of their success as disguise artists lies in their sophisticated “smart” skin.

Scattered throughout a cephalopod’s skin are thousands of small color organs called chromatophores, essentially little muscular, elastic sacs containing pigment. When muscular contractions stretch these pigment sacs into flat disks, a cephalopod’s skin is visibly colored or patterned. Individual or groups of chromatophores can be contracted at a time, creating an astonishing assortment of hues and designs. The cephalopods’ prowess as dress designers is not only impressive — it is also fast. In the blink of the eye, they may become striped, polka-dotted, or covered in psychedelic waves of color. An octopus may appear as if painted ruby red one minute and within seconds go ghostly pale or become a dull, mottled brown that replicates the underlying rock or sand bottom. The blue-ringed octopus can cause its namesake circular markings to flash brightly, and many cephalopods can create waves of color that wash over their bodies like a passing cloud. They can also produce patterns that disrupt the outlines of their bodies so that they become nearly unrecognizable. Surprisingly, their chromatophores contain only red, orange, yellow, black, or brown pigments, yet cephalopods exhibit a full rainbow of colors. The mystery of how they do this was solved when scientists discovered that they also have reflecting cells in their skin that act like mirrors or prisms. These iridophores and protein-based leucophores are used in combination with their chromatophores to create a wide variety of striking colors that include vibrant blues, purples, greens, and silver. How cephalopods respond so quickly and create so many patterns is, however, about more than just the color of their skin.

An intricate nervous system runs throughout a cephalopod’s epidermis, connecting its colored pigment organs and reflector cells to its relatively large brain and complex eyes. They are, in fact, the brainiest of all invertebrates, having the largest of the group along with especially well developed eyes. Hanlon’s research team has discovered that cephalopods use their exceptional vision as their primary means of detecting the brightness and patterns within their surroundings, which they then quickly replicate for camouflage. But, ironically, Hanlon’s team also found that most, if not all, cephalopods are color-blind. How then do they perfectly match the color of their surroundings? He suspects that the cephalopods’ skin has some sort of color-sensing capability, but what it is and how it works remain unknown.

As true masters of disguise, octopuses and cuttlefishes can also change the texture of their skin, creating bumps, ridges, or algae-like frills; this too appears to be a vision-based skill. Posing perfectly still or moving in an uncephalopod-like manner, they can imitate their surroundings in 3-D, becoming part of a rock, hiding among seaweed, or “impersonating” another organism. Octopuses have been seen to change their bodies to look and move like a flounder, a sea snake, or a drifting tumbleweed of algae. By hovering motionless and pointing their arms upward, a squid can be- come nearly unrecognizable within a stand of algae. Within the animal kingdom, the cephalopods’ rapid camouflage capabilities are simply the uncontested best. Even the iconic chameleons cannot match their speed or capabilities as quick-change artists.

Some cephalopods also have an illuminating means of camouflage. Using photophores or light organs on their undersides, squids can produce light that matches the radiance downwelling from above. This counter-illumination renders them invisible to predators looking up from below.

If camouflage fails, the cephalopods have several other tricks up their many suckered arms. They may attempt to bluff or startle an attacker with a display of flashing color, a rapidly changing pattern, or the release of ink. Many squids, octopuses, and cuttlefishes can eject ink as a smokescreen to facilitate a quick escape or as more of a decoy when released in combination with mucus to create a cephalopod-like shape. In the oceans’ darker depths, a cephalopod’s decoy or smokescreen may be bioluminescent. Some scientists speculate that this may provide an additional advantage: if an attacker gets smeared with glowing slime, it may go from stealthy predator to obvious prey, as the hunter becomes the hunted. Cephalopod ink may also irritate the eyes of other animals and chemically cause an attacker to become confused and disoriented. If camouflage or counter-measures don’t do the trick, cephalopods may exhibit erratic or unpredictable behavior in hopes of confusing predators. And if none of these tactics work and a hunter successfully nabs an arm or two, cephalopods are able to regenerate lost appendages. Some may even be able to lose a limb on command, if necessary.

The cephalopods’ exceptional shape-shifting and color-changing skills also provide an important means of communication. A certain posture or display may be used to attract mates or to ward off competing suitors. Color changes or positioning can signal aggression or lust, or sometimes both at the very same time. A male squid courting a female may blanch seductively on one side, while his other half darkens as a threat to watching rivals — literally exhibiting two moods at once.

In cephalopods the sexes are separate and they are all promiscuous. Fidelity has little place in their typically short lives; most live only one to two years. They are mainly seasonal breeders and often kick the proverbial bucket after reproduction. Some mate just once in a lifetime, while others get it on repeatedly during a single season, and a few species are able to reproduce throughout their ever-so brief lives.

Octopuses, for the most part, are solitary creatures and sex happens with little romance or foreplay. When a male octopus is ready and feels the need, he comes out into the open and may flash with color, display enlarged suckers or spread the web between his arms. But that is the extent of the preliminaries, as he may then leap on a nearby female or reach around to her from a distance with his specialized baby-maker arm. Male cephalopods are equipped with a characteristic arm that is designed especially for sex and used to transfer a package of sperm to females. Female octopuses are not always willing partners, though, and are known to often reject suitors. On rare occasions, multiple male octopuses may compete for a single female and more than one may try to mate with her at the same time. In that situation, eight arms might just come in handy. Because octopuses can be cannibalistic, small males must be wary when coming out into the open to mate — for them attraction truly can be fatal.

After mating, a female octopus typically lays her eggs in a den and stands guard. She gently jets water over her brood, keeping them clean and aerated, and forgoes food to ensure the safety and development of her eggs. Once they hatch, her parental duties are done; she is spent, and dies. Male octopuses tend to die at about the same age as the females. Theirs is the ultimate sacrifice for their young. But for at least one small, cold-water octopus, the female’s parental duties are not a fast finish to the end. Scientist James Wood at the Aquarium of the Pacific discovered that the female of the octopus Bathypolypus arcticus protects and broods her eggs for over a year, all the while wasting away as she metabolizes her own body to provide energy so that she can care for her offspring. This species, which lives in very cold water, is also unusual in that it can apparently live a relatively long life for a cephalopod, perhaps up to four, possibly even six years.

There are some octopuses that live in the open ocean and do not have dens at the seafloor in which to raise their young. In these species, females may carry their eggs cradled in their arms until their newborns emerge. The blanket octopus is one such species and spends its entire life drifting throughout the open ocean. It is an odd creature, even for an octopus, and has been likened to the caped crusader of the seas. It is typically dark pink, blue, or purple, with extended maroon webbing between its arms that trails behind it like a blanket or cape. And in this octopus, the sexes really are different — extremely different. The females may grow to be up to about 2 meters (6.5 feet) in length, whereas even mature males are just 2 to 3 centimeters (1 inch) long. Biologist Tom Tregenza at the University of Leeds likens it to a human-sized female mating with a male the size of a walnut. When it comes to pleasing their mates, however, the diminutive males of this species loom large and are especially self-sacrificing. During mating, the male blanket octopus not only passes a package of sperm to his mate using his specialized arm, he actually gives her part of the arm — it is detachable. Females have been found with the arms of numerous males in their mantles or body cavities. They are collectors of sperm and mates, at least of their body parts. After the male blanket octopus self-amputates part of his arm during sex, he dies. The males are the martyrs of their species, while the females sleep — that is, swim — around.

The diminutive males and immature females of the blanket octopus have also evolved a stunning way to deter predators. If a Portuguese man-of-war drifts by, they reach out and tear off a few tentacles, which they then carry clutched within their suckers at the ready for use in warding off attackers. Somehow, they too are immune to the man-of-war’s sting.

Reproduction in squids and cuttlefishes is distinctly different from that of the solitary, standoffish octopuses. During mating, male squids and cuttlefishes court and often guard their partners, at least temporarily. Also in contrast to the octopuses, female squids and cuttlefishes do not tend to their eggs once laid, and fertilization takes place externally. Most cuttlefishes breed in pairs or small groups over an extended area, but every winter in the rocky reefs of southern Australia, thousands of giant cuttlefish congregate in an unusual mass orgy of bottom-dwelling cephalopods. Hanlon’s team has spent hundreds of hours documenting this gathering and the associated reproductive behavior of the giant cuttlefish, which is unique to Australian waters. It has a flattened body that reaches up to about 50 centimeters (1.5 feet) in length, but with the extension of its eight thick arms and two feeding tentacles, it can appear even longer. Its eyes are big, and a ruffled fin surrounds its mantle or body. As with most of its kin, the giant cuttlefish also has exceptional color-changing and camouflage abilities.

Around late April, giant cuttlefish begin arriving at their breeding site in southern Australia, and by the peak of the gathering there may be over forty thousand individuals in the area. Among the gatherers there are more males than females, leading to intense competition for breeding partners. Most male rivalries are settled through aggressive displays or posturing, which signals their gender and readiness to fight. On rare occasions, the competition can get physical. Both sexes mate with multiple partners, their rendezvous brief. The females, however, have the upper arm, deciding which males get rejected and which get lucky. They may reveal their choice by arching their bodies in a rejection or spreading their blanched arms toward the males as an acceptance. At their first attempt, many male giant cuttlefish are sent packing. If not, a male spreads his arms and grasps the sides of a female’s head and she reciprocates, opening her arms and overlapping his in a sexual, but maybe not loving, embrace. The male jets water over the female’s private parts in an attempt to dislodge any sperm deposited by previous mates. Then, using his specialized arm, he makes his move, transferring a package of sperm to the female.

After copulation, the male giant cuttlefish alertly stands guard as the female readies to lay an egg, searching for the underside of a rock to deposit one of her brood. Other males may challenge the consort male or try to sneak in to plant their own seed. Hanlon’s team identified three tactics that these “sneaker” males use to get access to a female. They may simply hang around until a guarding male is distracted by a challenger or they might hide within a potential egg-laying site, lying in wait for an unsuspecting female to arrive. An even sneakier tactic is used by small males that hide their long baby-maker arms and adopt the coloration and posture of females. By appearing as members of the opposite sex, the small males lull the guarding males into a sense of security to get access to their mates, while also avoiding the aggression of other males. Some of these female “impersonators,” however, are a little too convincing for their own good, and males may begin to guard them or even try to mate with them.

During the annual orgy of the giant cuttlefish, females mate with multiple males and lay eggs at numerous locations. Each day in fact a female may mate seventeen times with from two to eight different males. From her eggs, miniature cuttlefish will hatch some three to five months later and have varying paternities. This reproductive strategy gives her offspring greater genetic variety, which increases the chance that some will survive. For the giant cuttlefish, the winter gathering will not be a repeat affair, because after just one breeding season they too take their last breath, swim their last swim — and die.

Less detail is known about the reproductive intimacies of many squid species, as it is more difficult to observe their midwater encounters. Since many squids live in schools during much of their lives, reproduction is often a group affair. Males compete for females, and both sexes appear to be promiscuous, taking on multiple partners throughout a breeding season. Squids may exhibit specific courtship rituals such as paired synchronized swimming or a flirtatious game of short-distance flee and pursuit. Color changes, patterning, and arm positioning are used to signal desire, rejection, or aggression. Small male squids also exhibit “sneaker” tactics to get access to females guarded by larger males. Squid sex seems to be exceptionally brief, and it may only take seconds for a male to transfer his sperm to a female (plate 14). They produce gelatinous egg masses that may lie aggregated at the seabed or attach to a substrate or float within the water. Clusters of jelly-encased eggs can appear mop-like at the bottom or resemble large, white, elongated capsules. Depending on the species, a single female squid may produce well over a hundred thousand eggs. Incubation time varies between species and also depends on size and water temperature. Squids do not tend to their eggs, and hatchlings from a single brood may have multiple paternities as in the cuttlefishes. In some cases, there may be a large-scale mass mortality after breeding, resulting in the parents’ corpses lying among their eggs at the seafloor, the previous generation amid the promise of the next. And cephalopods become hunters very early on; within just a day or so of hatching, baby squids and other cephalopods are already capable of capturing prey, albeit small to start.

As a group, the cephalopods are diverse and include some pretty strange characters, many of which live in deep, difficult-to-access marine environments. As Wood puts it, “They are not rare creatures, just rarely seen and seldom studied.” Of course the most infamous example of this is the giant squid. Even though it is one of the largest animals on the planet, possibly reaching an overall length of some 18 meters (60 feet), to date it has been caught on film, momentarily, only once, in 2005. Like other cephalopods, giant squid are believed to grow fast, and may attain their immense size in just a few years. They are thought to occur throughout the world’s oceans and inhabit depths mainly between 300 and 1,000 meters (980 and 3,280 feet). What we know about this huge and mysterious creature comes mostly from specimens caught in fishing trawls or that have washed ashore dead. For years, debate has raged over whether the giant squid is a strong, muscular, and fast predator or more of an oversized weakling. Their reputation as being a bit on the limp side stems from the fact that their arms and bodies, like those of many mid- and deep-water squids, are known to contain a solution of ammonium chloride, which helps to keep them neutrally buoyant. Many scientists, however, are rethinking the weakling theory based on the giant squid’s one on-air appearance, in which it at- tacked and dragged a heavily laden cable. As for giant squid sex; scientists hypothesize that the females may store the males’ sperm under their arms (female cephalopods often store sperm not only in their reproductive tracts, but also on their heads, arms, bodies, and around their mouths), and that while the male has a specialized arm for sperm transfer, he may also have a 1 meter (3 feet) long penis. How, where, and when they mate remains unknown. The giant squid appears to feed mainly on deep-water fishes and other cephalopods. Because of its fast growth rate and size, its predators are thought to be limited mainly to toothed whales, in particular the sperm whale. Reports of the two fighting it out, though, seem a bit far-fetched, as once caught, the giant squid is probably quickly bested by the powerfully built whale.

In the oceans’ mid- and deep-water realms there are many cephalopod oddities. One such creature is the cock-eyed squid, resembling a giant strawberry with bizarre, asymmetrical eyes. Its richly red body is covered with tiny rows of photophores (light organs), and one of its eyes is small, bluish, and sunken within its head, while the other is larger, yellowish, and sticks out. Another strange-eyed midwater squid has one large eye looking up and a smaller eye directed downward. It can simultaneously be on the lookout for predators above as well as below. Now there is a morphology that would come in handy before crossing a busy street. During a 2005 Arctic cruise for the Census of Marine Life program, cephalopod expert Ron O’Dor observed another armed oddity, noting, “Its fins flap slowly when it swims. It looks like Dumbo.” The bright pink, large-finned octopus with webbed arms made headlines as — what else — the Dumbo octopus.

In the dark depths of the temperate and tropical oceans, some 600 to 1,200 meters (1,900 to 3,900 feet) down, lives what may be the strangest of all the cephalopods. It has a velvety dark body, webbed arms, and large, ball-like eyes that glow blue or red in the light. Named Vampyroteuthis infernalis, or the vampire squid from hell, it is a unique “multiethnic” cephalopod with the combined characteristics of a squid, octopus, and cuttlefish. The vampire squid, however, is not a blood-thirsty predator as its name suggests, but rather a big softy that fishes using its own reels and retractable lines. Its body resembles a large, soft, brown or black foot- ball outfitted with eight suckered, webbed arms that have small fingerlike projections on their undersides. The vampire squid also has two unique tentacle-like filaments that are thin and elastic, and can be deployed like fishing lines. When reeled in, its filaments are tucked away within two small pockets between its arms. Young vampire squid use jet propulsion to get around, but as they get older, they appear to rely more heavily on the flapping of their two rounded, stubby fins. These fins develop as they mature and take the place of smaller baby fins that get reabsorbed back into their bodies. The arms of the vampire squid are especially peculiar, tipped with unusual light organs that can glow or pulse or release a thick sticky fluid containing bioluminescent particles — that is, they have arms that can fire beads of glowing slime. When the arms all fire at once, a shimmering cloud envelops the vampire squid, presumably as a defensive strategy. Researchers have also observed the vampire squid in an inexplicable and curious feat of undersea acrobatics. It swings its webbed arms up and over its head, essentially turning itself inside out, with its suckers and associated fingerlike protrusions sticking out. Witnessing this odd behavior, biologist Bruce Robison at the Monterey Bay Aquarium Research Institute describes them as going from “a soft football into a spiky pineapple with a glowing top.” He believes they can see through their arms’ thin webbing in this position, but why they turn themselves inside out remains a mystery. The vampire squid appears to feed mainly on small crustaceans and likes to hang out in zones of low oxygen. Staying in poorly oxygenated waters may be a means for it to avoid faster predators that have a higher metabolism and are less capable of absorbing oxygen as efficiently as they do.

Among the cephalopods, there is only one that still has the outer shell of its distant relatives. The nautilus is an oddly beautiful creature that resides within a coiled, pearly shell that the ancient Greeks considered a symbol of perfection. It has large, simple pinhole eyes and some ninety suckerless arms, and is found only in the warm waters of the Indo-Pacific down to depths of about 500 meters (1,640 feet), often along the steep slope of a reef front. Scientists believe they cannot go deeper than about 700 meters (2,200 feet) or their shells would implode. The nautilus uses its shell as both a refuge and as an unusual device for buoyancy control. If threatened, the soft-bodied nautilus can withdraw into its casing and cover the opening with a tough, leathery hood. Its home is done in camouflage with countershaded coloration, having chocolate-brown or rust- colored stripes on the top and a white underside. The shell is chambered and the nautilus resides in the last or most recently constructed section. The other chambers are filled with either fluid or gas. By adjusting the amount of gas versus fluid in its shell, the nautilus can control its buoyancy and float neutrally. It swims by retracting its body into its shell to create an awkward and weak form of jet propulsion. Unlike the others of its clan, this cephalopod’s vision is poor, so it must rely more heavily on smell and touch to scavenge for food. The nautilus seems to dine preferentially on crustaceans and often migrates into shallower waters at night in search of a meal. Instead of just one specialized arm for sex, the male nautilus has several arm designates that are used in reproduction. Observations suggest that the males are indiscriminating and easily confused when it comes to the mating game. They will apparently approach and try to have sex with just about anything that appears nautilus-like. And once a male nautilus successfully identifies a female — of his own kind — he is undaunted if she lacks interest, grabbing and sometimes biting his feisty companion into a tryst that may go on for hours. For the nautilus, it is not just one season of sex and then death; they are able to mate over multiple years. This is partly because, for a cephalopod, the nautilus lives a surprisingly long life, perhaps growing as old as twenty.